Post‐fire pickings: Large herbivores alter understory vegetation communities in a coastal eucalypt forest

Abstract Fire and herbivores alter vegetation structure and function. Future fire activity is predicted to increase, and quantifying changes in vegetation communities arising from post‐fire herbivory is needed to better manage natural environments. We investigated the effects of post‐fire herbivory on understory plant communities in a coastal eucalypt forest in southeastern Australia. We quantified herbivore activity, understory plant diversity, and dominant plant morphology following a wildfire in 2017 using two sizes of exclosures. Statistical analysis incorporated the effect of exclusion treatments, time since fire, and the effect of a previous prescribed burn. Exclusion treatments altered herbivore activity, but time since fire did not. Herbivory reduced plant species richness, diversity, and evenness and promoted the dominance of the most abundant plants within the understory. Increasing time since fire reduced community diversity and evenness and influenced morphological changes to the dominant understory plant species, increasing size and dead material while decreasing abundance. We found the legacy effects of a previous prescribed burn had no effect on herbivores or vegetation within our study. Foraging by large herbivores resulted in a depauperate vegetation community. As post‐fire herbivory can alter vegetation communities, we postulate that management burning practices may exacerbate herbivore impacts. Future fire management strategies to minimize herbivore‐mediated alterations to understory vegetation could include aggregating management burns into larger fire sizes or linking fire management with herbivore management. Restricting herbivore access following fire (planned or otherwise) can encourage a more diverse and species‐rich understory plant community. Future research should aim to determine how vegetation change from post‐fire herbivory contributes to future fire risk.

plant diversity, and dominant plant morphology following a wildfire in 2017 using two sizes of exclosures. Statistical analysis incorporated the effect of exclusion treatments, time since fire, and the effect of a previous prescribed burn. Exclusion treatments altered herbivore activity, but time since fire did not. Herbivory reduced plant species richness, diversity, and evenness and promoted the dominance of the most abundant plants within the understory. Increasing time since fire reduced community diversity and evenness and influenced morphological changes to the dominant understory plant species, increasing size and dead material while decreasing abundance. We found the legacy effects of a previous prescribed burn had no effect on herbivores or vegetation within our study. Foraging by large herbivores resulted in a depauperate vegetation community. As post-fire herbivory can alter vegetation communities, we postulate that management burning practices may exacerbate herbivore impacts.
Future fire management strategies to minimize herbivore-mediated alterations to understory vegetation could include aggregating management burns into larger fire sizes or linking fire management with herbivore management. Restricting herbivore access following fire (planned or otherwise) can encourage a more diverse and species-rich understory plant community. Future research should aim to determine how vegetation change from post-fire herbivory contributes to future fire risk.

K E Y W O R D S
herbivory, large herbivore, macropod, post-fire, vegetation community

T A X O N O M Y C L A S S I F I C A T I O N
Biodiversity ecology

| INTRODUC TI ON
Fire and herbivores are consumers of vegetation, modifying the structure and function of plant communities (Bond & Keeley, 2005).
Interactions between these disturbances can occur in ecosystems where both fire and herbivores are prevalent. However, few studies have implemented manipulative field studies to measure the long-term responses of forest vegetation to both fire and herbivory (Foster et al., 2016;Nuttle et al., 2013;Royo & Carson, 2006). As forest ecosystems are likely to face increased fire activity in the future (Bowman et al., 2009), more research that quantifies interactions between fire and herbivory on plant communities is required.
Fire can encourage or deter herbivore foraging (Allred et al., 2011;Fuhlendorf et al., 2010). Research into fire-herbivore relationships, under the banner of "pyric herbivory," has emphasized the capacity for fire to influence foraging selection by herbivores (Allred et al., 2011). Large herbivores (>2 kg) can be attracted to burnt patches due to increased abundance of new growth and more favorable physical or chemical accessibility to food (Allred et al., 2011;Danell et al., 2006;Foster et al., 2016). However, limited research has been conducted on the next logical question within fire-prone ecosystems, which is: How does the vegetation community respond when it is burnt, and then foraged? Manipulative experiments are required to answer this question ( Figure 1).

Information on changes in vegetation communities arising from
post-fire herbivory may guide future fire management practices.
Large herbivores can alter plant succession following a fire through foraging, trampling, and alterations in nutrients (by defecation, urination, decomposition of carcasses, etc.; Forbes et al., 2019;Persson et al., 2000). Herbivores actively select for more palatable species, which leads to the dominance of unpalatable, chemically defended plant species, or an increased abundance of highly palatable plants through nutrient cycling and seed dispersal (Augustine & McNaughton, 1998;Bakker et al., 2016;Leroux et al., 2020).
Changes to aboveground plant biomass is a direct modification of in situ fuel load (Archibald & Hempson, 2016). Fire also can promote the abundance of more flammable plants (through positive feedback loops) that are often less palatable for herbivores (due to lower moisture content, increased tannins/oils, higher carbon-nitrogen ratios, etc.; Archibald & Hempson, 2016). As dominant plant species can influence fire risk (Cheney et al., 2012;Zylstra et al., 2016), quantifying the changes to plant communities from post-fire herbivory will be paramount to future wildfire management and predictions ( Figure 2).
We aimed to answer the question: How does post-fire herbivory alter understory plant communities and physical attributes of the dominant plants in a eucalypt forest? We used a manipulative field study at Booderee National Park that modified large herbivore activity through different levels of fencing. At all plots, we tested the effects of fencing treatments and time since fire on herbivore activity, vegetation community measures, and morphological responses of the dominant understory plant. Where applicable, we also investigated the effect of the previous prescribed burn (5 years prior) applied to selected plots. We expected large herbivores to be attracted to recently burnt areas due to the availability of fresh growth and herbivore occurrence would decline over time as the vegetation regenerates (Allred et al., 2011). This response has been observed following prescribed burns in eucalypt forest (Foster et al., 2015;Parkins et al., 2019). However, it is possible that this effect will be less evident following a larger wildfire where herbivores have a larger area of burnt space to select from.
While fire can reduce habitat complexity (Parkins et al., 2019), the interaction of fire and (increased) herbivory may result in an altered vegetation community with reduced species diversity (Foster et al., 2015). Fire will promote germination and growth of understory plants, resulting in a short-term increase in species richness (Ross et al., 2002). Species richness within the understory plant community typically decreases with time since fire due to increased competition and reduced space (Foster et al., 2018). Large herbivores can dramatically alter the recovering understory vegetative community by preferentially selecting the more palatable species (Persson et al., 2000). We expect that this should result in a decrease in community measures such as richness, diversity, and evenness and promote the dominance of less palatable plants F I G U R E 1 Large herbivores present in our study, the (a) swamp wallaby (Wallabia bicolor) and the (b) eastern grey kangaroo (Macropus giganteus). Photo credit: C. N.
within burnt patches (Foster et al., 2016). In addition, we expect the influence of the prior prescribed burn to exacerbate herbivore impacts following a wildfire as the vegetation has been subject to a short (5 years) fire interval and may be more sensitive to further disturbance compared to areas that were not subject to the prescribed burn (Furlaud et al., 2018).
A particular concern for managers of our study area has been the increase in dominance of the fern Pteridium esculentum (bracken) in the understory vegetation (Dexter et al., 2013).
Current management of Booderee National Park is based on the understanding that abundant large herbivore populations, coupled with recurrent fires (prescribed burns and wildfires), are promoting bracken dominance (Dexter et al., 2013). Bracken has reduced palatability for larger herbivores (Di Stefano & Newell, 2008) and is an early-successional and fire-resistant plant (Tolhurst & Turvey, 1992). The ramifications for both biodiversity and future fire risk resulting from a bracken-dominated understory are currently unknown. We aimed to provide quantitative evidence on the effect that post-fire herbivory has on the morphology and abundance of bracken.
By focusing our study in a post-wildfire eucalypt forest, we pre-
No other large terrestrial herbivore species are currently found in Booderee National Park. All three macropods have previously demonstrated pyric herbivory responses with most studies identifying a preference for recently burnt patches due to a higher quality of foraging resources (Foster et al., 2015;Meers & Adams, 2003;Parkins et al., 2019;.

F I G U R E 2
Hypothesised outcomes of foraging from large herbivores following a fire event in a eucalypt forest environment Of the three macropod species, the eastern grey kangaroo and the swamp wallaby are the most common in Booderee National Park (Chard et al., 2021). While density measures have not been conducted for any macropod species, previous research analyzing conditional abundance of the swamp wallaby peaked between 2007 and 2013 compared to when surveys began in 2003 (Lindenmayer et al., 2016). Furthermore, managers have been concerned with the growing population of macropods in Booderee National Park (Dexter et al., 2013). Previous research in the study area found both species preferentially selected forest vegetation communities (Chard et al., 2021). The eastern grey kangaroo is a grazing species, targeting grass species such as Imperata cylindrica and Themeda triandra (Brunton et al., 2018). The swamp wallaby is a browsing species that will forage on most understory plants in a forest community with a preference for forb species (Di Stefano & Newell, 2008).

| Study design
We quantified the interacting effects of post-fire herbivory on vegetation communities using two randomized, blocked experi- plots (4 ha, hereafter referred to as "large" plots) in forest vegetation. Large plots were spaced 300 m apart and blocks at least 2 km apart. Again, we manipulated herbivore grazing pressure using two randomly allocated fencing treatments: (1) open (no fencing) and (2) closed (completely fenced).

| Data collection
We conducted scat surveys every 2 months from October 2018 to February 2020 in all plots, within two 25 m × 2 m transects (small plots), and four 50 m × 2 m transects (large plots), in which macropod scats were counted and removed from the transect. We used macropod scat counts as an index of herbivore activity, as macropods defecate primarily while feeding (Johnson et al., 1987;Murphy & Bowman, 2007). Note, it was assumed in this study that macropods will digest and deposit all vegetation at a similar rate.
We conducted vegetation surveys annually in spring, in all plots. We

| Data analysis
We analyzed the influence of exclosure fences, time since fire, and the 2012 prescribed burn on: (1) scat counts, (2) plant community measures, and (3) bracken attributes in R (R Core Team, 2016). We fit models from a candidate set of nine models (small plots) and two models (large plots) for each response in a Bayesian framework using the "brms" package (Bürkner, 2017). The models we constructed used all possible combinations of exclusion treatment (open/partial/ closed), time since fire, and prescribed burn (burnt/unburnt) for each response variable (Tables S1-S3). We selected appropriate regression distributions for each variable after testing for assumptions of normality and homogeneity of variance (see Tables S1; Tables 2   and 3; Hanea et al., 2015).
Our response variables were as follows: (1) number of macropod scats, with scat counts being summed at 2-month intervals for small plots to allow for effective analysis of the partial treatments (as every second count was effectively zero); (2) understory plant richness, diversity, evenness, and dominance, with vegetation measures calculated using the "diversityresult" function from the "BiodiversityR" package (Kindt & Kindt, 2019); and (3) bracken width, height to bottom frond, top height, count of individuals, and percentage of dead material. We treated time since fire as a continuous variable for scat surveys, standardized using the "scale" function so that the mean was zero with a standard deviation of 1. We included season (for scat surveys) and block as a fixed effect in each model as well as the random effect of plot. We expected a seasonal effect resulting in reduced herbivore activity in the summer months as macropod defecation rates decrease and scat decay increases (Perry & Braysher, 1986). We selected appropriate priors for each model and the Rhat values were deemed acceptable (all values = 1; Gelman & Rubin, 1992).
The models were fit using Markov chain Monte Carlo methods.
We ran four chains, each with 3000 iterations with the first 1000 iterations discarded as burn-in for the sampler. We based our inference on the importance of the hypothesized interactions by selecting the most parsimonious model using lowest weighted Akaike information criterion (WAIC; ≤2) and simplest model using the "loo" package (Burnham & Anderson, 2002;Vehtari et al., 2017). We selected AIC over the Bayesian information criterion (BIC) to allow the inclusion of more potential predictors in the model (Aho et al., 2014).
We present results for most parsimonious models for macropod scats, vegetation community measures, and bracken morphology from small and large plots.

| Herbivore activity
Our exclosure treatments altered herbivore activity ( Table 1). The best performing model for both small and large plots did not include any interaction terms (Table S1). In both small and large plots, scat counts were highest in the open treatment and lowest in the closed treatments ( Figure 4). We found in the small plots that partial treatments had scat counts at intermediate levels between open and closed treatments. Time since fire did not influence herbivore activity in either large or small plots. Furthermore, we detected no effect of the previous prescribed burns in the small plots. Season only affected scat counts within the large plots, with counts being lower in summer months. Notably, scat counts in the large, closed plots were not zero (11.9 ± 6.5 SE), indicating some level of macropod intrusion within the exclosure fences ( Figure 4).

| Vegetation community
Three years of vegetation surveys yielded 74 plant species in the understory community. We found herbivore activity and time since fire altered understory community measures in both small and large plots ( Figures 5 and 6).
In small plots, the interaction of herbivory and time since fire was included in the selected models for diversity and dominance (Table   S1). However, the confidence intervals for both interaction effects overlapped with zero indicating a weak effect (Table 2) In large plots, the interaction of herbivory and time since fire was included in richness, diversity, and evenness models (Table S2). The confidence intervals for the interaction effect for species richness overlapped with zero ( Table 3). We observed comparable trends to

| Dominant plant morphology
During the 3 years of vegetation surveys, we measured 3468 individual P. esculentum plants. The interaction effect of herbivore  (Table S3)

| DISCUSS ION
The interactive effect of herbivory and fire on vegetation structure, composition, and dynamics is important but often overlooked  Year (

Count
Est.

Count
Est.

CI (95%)
Intercept  Dexter et al., 2013;0.25 ha, Foster et al., 2015;and 714 ha, Hradsky et al., 2017). Macropods may be selecting for burnt patches within our study area but, due to the large size of the 2017 wildfire, increased occurrence may have been distributed over a large area, resulting in only a nuanced effect at our study plots. If fire size is impacting herbivore response, future prescribed burning practices may need to accommodate local herbivore density. To confirm this, more investigations would be required to determine the relationship between fire size and herbivore density.

| Shifting vegetation communities
Knowledge of modifications to vegetation communities by large herbivores within fire-prone ecosystems is increasing (Crowther et al., 2016;Tuft et al., 2012). We found that post-fire herbivory reduced plant species richness, diversity, and evenness and increased plant dominance measures. This was expected as foraging pressure by large herbivores has been shown to decrease diversity and increase species dominance in other ecosystems (Bakker et al., 2006;Connor et al., 2021;Tuft et al., 2012). This finding confirms that increased foraging pressure from large herbivores following a wildfire also results in a more depauperate vegetation community, consistent with previous studies of smaller prescribed/experimental burns (Foster et al., 2015;Parkins et al., 2019).
Our study revealed that the richest and most diverse plant communities occurred directly after fire. These findings are consistent with earlier studies indicating richness decreases with increasing time since fire (Foster et al., 2018;Ross et al., 2002). Higher species richness immediately after fire was expected in eucalypt forest understory as fire typically stimulates new growth and the germination of seedlings, and many species can re-sprout after fire (Dixon et al., 2018). Furthermore, within large plots, we observed that with increasing time since fire, herbivore exclusion promoted a more diverse and more even community. Preventing large herbivores from accessing burnt patches may therefore promote a richer and more diverse understory.

| Morphology of bracken
The increase in P. esculentum dominance within Booderee National Park has been an ongoing concern for resource managers (Dexter et al., 2013). However, this study did not uncover evidence of differences in bracken morphology with altered herbivore activity.  (Cheney et al., 2012). However, no changes were observed within the large plots. Potential differences in our results may be due to the difference between time since exclosure (9 years vs. 3 years) or the time to establishing the larger manipulative experiment following the wildfire in 2017 (10 months). The latter effect may have allowed macropods to modify the understory before the fences affected herbivore activity, reducing the contrast between plots.
Extending the survey to future years may reveal important findings as dead biomass of bracken usually peaks at 4 to 7 years following disturbance (Bray, 1991;Parkins et al., 2019). Longer-term datasets (>3 years) may be required to document post-fire bracken growth within forested communities.

| Fire history
We found no evidence that previous prescribed burns in 2012 in- where impacts on slower growing species, and in particular obligate seeding shrub species, become easier to detect.

| CON CLUS ION
Our study highlights the impacts of post-fire herbivory on vegetation communities. Post-fire herbivory decreases richness, diversity, and evenness measures and increases the dominance of few species leading to a more depauperate vegetation community. Future management of forest ecosystems should account for local populations of large herbivores. Increased understory plant diversity may be achieved by reducing herbivore numbers or preventing access to burnt patches following fire. Conversely, where herbivore impacts align with management goals (e.g., control of palatable weeds, or reducing fuel biomass for fire hazard reduction), small prescribed burns may be effective in concentrating foraging pressure by herbivores in target areas.

ACK N OWLED G EM ENTS
We acknowledge the traditional owners of the land, the Wreck Bay Indigenous Community, on which our research was conducted. We thank the Wreck Bay Aboriginal Community Council and Parks Australia for supporting this project and assisting with the construction of the exclosure fences. This research was supported by the Australian Research Council, Parks Australia, and the Australian Department of Defence as part of an ARC Linkage Project (LP170100152). We thank the staff of Booderee National Park who conducted prescribed burns. We would also like to thank those who assisted in the construction of exclosures and data collection: Dylan Cook, Ruth Hollows, Milou Hofman, Sophia Cain, Sean Evans, and Bud Hopkins.

CO N FLI C T S O F I NTE R E S T
The authors declare no conflicts of interest.

O PEN R E S E A RCH BA D G E S
This article has earned an Open Data Badge for making publicly available the digitally-shareable data necessary to reproduce the reported results. The data is available at https://datad ryad.org/stash/ share/ PRjYH am6K3 TZZ-9-ZDOc9 6p1qN zDOH8 yXz19 6j1RLuI.

DATA AVA I L A B I L I T Y S TAT E M E N T
The data that support the findings of this study are openly available in Dryad using the digital object identifier (DOI): https://doi.